Supramolecular Organization of the Repetitive Backbone Unit of the Streptococcus pneumoniae Pilus

Spraggon, Glen; Koesema, Eric; Scarselli, Maria; Malito, Enrico; Biagini, Massimiliano; Norais, Nathalie; Emolo, Carla; Barocchi, Michèle Anne; Giusti, Fabiola; Hilleringmann, Markus; Rappuoli, Rino; Lesley, Scott; Covacci, Antonello; Masignani, Vega; Ferlenghi, Ilaria

doi:10.1371/journal.pone.0010919

Title: Supramolecular Organization of the Repetitive Backbone Unit of the Streptococcus pneumoniae Pilus

Journal Article · 15 June 2010 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0010919 · OSTI ID:1627409

Spraggon, Glen ^[1]; Koesema, Eric ^[2]; Scarselli, Maria ^[3]; Malito, Enrico ^[4]; Biagini, Massimiliano ^[3]; Norais, Nathalie ^[3]; Emolo, Carla ^[3]; Barocchi, Michèle Anne ^[3]; Giusti, Fabiola ^[5]; Hilleringmann, Markus ^[3]; Rappuoli, Rino ^[3]; Lesley, Scott ^[2]; Covacci, Antonello ^[3]; Masignani, Vega ^[3]; Ferlenghi, Ilaria ^[3]

Genomics Inst. of the Novartis Research Foundation, San Diego, CA (United States); DOE/OSTI
Genomics Inst. of the Novartis Research Foundation, San Diego, CA (United States)
Novartis Vaccines and Diagnostics, Siena (Italy)
Genomics Inst. of the Novartis Research Foundation, San Diego, CA (United States); Novartis Vaccines and Diagnostics, Siena (Italy)
Univ. of Siena (Italy). Dept. of Evolutionary Biology

Streptococcus pneumoniae, like many other Gram-positive bacteria, assembles long filamentous pili on their surface through which they adhere to host cells. Pneumococcal pili are formed by a backbone, consisting of the repetition of the major component RrgB, and two accessory proteins (RrgA and RrgC). Here we reconstruct by transmission electron microscopy and single particle image reconstruction method the three dimensional arrangement of two neighbouring RrgB molecules, which represent the minimal repetitive structural domain of the native pilus. The crystal structure of the D2-D4 domains of RrgB was solved at 1.6 Å resolution. Rigid-body fitting of the X-ray coordinates into the electron density map enabled us to define the arrangement of the backbone subunits into the S. pneumoniae native pilus. The quantitative fitting provide evidence that the pneumococcal pilus consists uniquely of RrgB monomers assembled in a head-to-tail organization. The presence of short intra-subunit linker regions connecting neighbouring domains provides the molecular basis for the intrinsic pilus flexibility.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC03-76SF00098

OSTI ID:: 1627409

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 6 Vol. 5; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Complete Genome Sequence of a Virulent Isolate of Streptococcus pneumoniae Tettelin, H. Science, Vol. 293, Issue 5529 https://doi.org/10.1126/science.1061217	journal	July 2001
Genome Analysis Reveals Pili in Group B Streptococcus Lauer, P. Science, Vol. 309, Issue 5731 https://doi.org/10.1126/science.1111563	journal	July 2005
Stabilizing Isopeptide Bonds Revealed in Gram-Positive Bacterial Pilus Structure Kang, H. J.; Coulibaly, F.; Clow, F. Science, Vol. 318, Issue 5856 https://doi.org/10.1126/science.1145806	journal	December 2007
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Type IV Pilus-Dependent Motility and Its Possible Role in Bacterial Pathogenesis Shi, Wenyuan; Sun, Hong Infection and Immunity, Vol. 70, Issue 1 https://doi.org/10.1128/IAI.70.1.1-4.2002	journal	January 2002
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A Second Pilus Type in Streptococcus pneumoniae Is Prevalent in Emerging Serotypes and Mediates Adhesion to Host Cells Bagnoli, Fabio; Moschioni, Monica; Donati, Claudio Journal of Bacteriology, Vol. 190, Issue 15 https://doi.org/10.1128/JB.00384-08	journal	May 2008
Group B Streptococcal Pilus Proteins Contribute to Adherence to and Invasion of Brain Microvascular Endothelial Cells Maisey, Heather C.; Hensler, Mary; Nizet, Victor Journal of Bacteriology, Vol. 189, Issue 4 https://doi.org/10.1128/JB.01153-06	journal	October 2006
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Pneumococcal Pili Are Composed of Protofilaments Exposing Adhesive Clusters of Rrg A Hilleringmann, Markus; Giusti, Fabiola; Baudner, Barbara C. PLoS Pathogens, Vol. 4, Issue 3 https://doi.org/10.1371/journal.ppat.1000026	journal	March 2008
Dual Role for Pilus in Adherence to Epithelial Cells and Biofilm Formation in Streptococcus agalactiae Konto-Ghiorghi, Yoan; Mairey, Emilie; Mallet, Adeline PLoS Pathogens, Vol. 5, Issue 5 https://doi.org/10.1371/journal.ppat.1000422	journal	May 2009

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Expression of the Type 1 Pneumococcal Pilus Is Bistable and Negatively Regulated by the Structural Component RrgA Basset, Alan; Turner, Keith H.; Boush, Elizabeth Infection and Immunity, Vol. 79, Issue 8 https://doi.org/10.1128/iai.05117-11	journal	May 2011
The Pilin Protein FimP from Actinomyces oris: Crystal Structure and Sequence Analyses Persson, Karina; Esberg, Anders; Claesson, Rolf PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0048364	journal	October 2012
Protective Activity of the CnaBE3 Domain Conserved among Staphylococcus aureus Sdr Proteins Becherelli, Marco; Prachi, Prachi; Viciani, Elisa PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0074718	journal	September 2013
Plasmid Characterization and Chromosome Analysis of Two netF+ Clostridium perfringens Isolates Associated with Foal and Canine Necrotizing Enteritis Mehdizadeh Gohari, Iman; Kropinski, Andrew M.; Weese, Scott J. PLOS ONE, Vol. 11, Issue 2 https://doi.org/10.1371/journal.pone.0148344	journal	February 2016
Current status and perspectives on protein-based pneumococcal vaccines Darrieux, Michelle; Goulart, Cibelly; Briles, David Critical Reviews in Microbiology, Vol. 41, Issue 2 https://doi.org/10.3109/1040841x.2013.813902	journal	July 2013

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